Seasonal differences in the physiology of Carcinus maenas (Crustacea: Decapoda) from estuaries with varying levels of anthropogenic contamination

Abstract

This study reports the seasonal variability in aspects of the physiology of the shore crab Carcinus maenas from three estuaries in South-west England, each with varying anthropogenic inputs: Avon Estuary (‘relatively low’ impact), Yealm Estuary (‘intermediate’ impact) and Plym Estuary (‘relatively high’ impact). Crabs collected over 12 months from the Avon had a significantly ‘lower’ physiological condition in winter and spring compared to summer and autumn; in particular, haemocyte phagocytic capability (a general indicator of immune function) was significantly higher in winter and spring compared to summer and autumn, and total haemolymph antioxidant status (an indicator of oxidative stress) was significantly lower in winter compared to the remainder of the year. Potentially, shore crabs may be more susceptible to the effects of contaminant exposure, such as increased immunotoxicity (thus, reduction of immune function) and/or oxyradicals (or reactive oxygen species) exposure) especially in seasons of increased susceptibility i.e. summer/autumn (lower phagocytic capability) and winter (lowest antioxidant function). As the Avon was taken to represent the ‘reference’ site, this pattern is considered to reflect the ‘normal’ seasonal variability in shore crab physiology. Shore crab physiological condition from the ‘relatively high’ impact estuary (Plym) revealed increased cellular viability and antioxidant status in autumn and winter compared with that of the ‘standard’ pattern (Avon) However, crabs from the intermediate impact estuary (Yealm) only demonstrated significant physiological differences in summer as shown by a lower cellular viability. All crabs had been exposed to PAHs (confirmed by the presence of PAH metabolites in their urine) which may account for the observed differences in shore crab physiology. In conclusion, to aid understanding of the potential contaminant impacts on biota it is imperative that the ’normal’ seasonal variability of physiological condition be established. Biological effects-based monitoring studies should therefore be employed seasonally to potentially highlight ‘windows of sensitivity’ to contaminant impact.

Introduction

Coastal marine waters and sediments, including estuaries, continually receive anthropogenic inputs and contain many chemicals that are potentially toxic to aquatic organisms (Ridgway and Shimmield, 2002, Salazar-Coria et al., 2010). Accelerated human population growth and development around these coastal and estuarine zones have placed pressure on these sensitive habitats, such as eutrophication, decreased biodiversity, habitat loss and alteration (Kennish, 2002), especially as these coastal areas are deemed ‘ecological nurseries’ where the most sensitive juvenile life-stages of organisms are found (Haywood et al., 1998, Epifanio et al., 2003, Moksnes et al., 2003). The recent emphasis of marine environmental monitoring has been to develop biological measurements of anthropogenic impact, including physiological assessments of the ‘health’ of chosen test species (Galloway et al., 2002, Galloway et al., 2004, Galloway et al., 2006). Unfortunately, implementation of this approach is impeded by the lack of knowledge of the basic biochemistry of the organisms, including “normal” physiological ranges, such as seasonal variations (Mehrle and Mayer, 1980) before the impact of polluting chemicals can be assessed. Seasonal patterns are summarised as temporal variations which are “usually responses to particular cues that tend to coincide with time of year, if such cues do not arise in any particular year, the response will not be elicited” (Crowe, 1999).

The shore crab Carcinus maenas (Decapoda: Brachyura) is a common inhabitant of various coastal habitats, including estuaries (Crothers, 1968, Hunter and Naylor, 1993), throughout Europe (Hayward and Ryland, 1995), and is used widely as a test organism in ecotoxicology (Bamber and Depledge, 1997b, Fossi et al., 2000). C. maenas responds quickly to environmental change, through changes in osmoregulation (Bjerregaard and Visle, 1985, Bjerregaard and Vislie, 1986), respiration rates and capability (Arudpragasm and Naylor, 1964a, Arudpragasm and Naylor, 1964b, Dawirs, 1983, Depledge, 1985, Spicer and Weber, 1991), and metabolic and cardiac activity (Wallace, 1972, Cumberlidge and Uglow, 1977a, Cumberlidge and Uglow, 1977b, Depledge, 1984). The physiological plasticity of C. maenas is a major factor accounting for its widespread distribution (Rainbow, 1997). However, low genetic variability has been shown for shore crab populations around the U.K. coasts, indicating that patterns of phenotypic variability among shore crab populations are likely to reflect differences between local environments (Brian et al., 2006), making this species a good bioindicator of environmental contamination. Shore crab ‘health’ assessments using various physiological techniques (including cellular viability and immune function) have been employed previously in both laboratory and field scenarios demonstrating contaminant impact this species (Brown et al., 2004, Galloway et al., 2004, Hagger et al., 2009). The aims of this present study were, therefore, to firstly, elucidate the ‘natural’ seasonal pattern in shore crab physiology in crabs from a relatively clean estuary (Avon Estuary) and secondly, to evaluate whether such seasonal patterns were altered under conditions of anthropogenic input i.e. maritime activity i.e. ‘intermediate’ Yealm Estuary and ‘relatively high’ Plym Estuary.